Spontaneous male death during copulation in an orb-weaving spider

Abstract

Males of some cannibalistic species of spiders and insects appear to sacrifice themselves by allowing the female to eat them, and the adaptive significance of such drastic terminal reproductive investment has recently been demonstrated for a spider. Typically, the female has to kill the male, but it has been suggested that males of some species in the cannibalistic orb-weaving spider genus Argiope may die in copula without female 'collaboration'. Here, we provide the first experimental evidence to our knowledge of programmed sudden death after onset of copulation in males of the spider Argiope aurantia. Our observations reveal that males invariably die during the insertion of their second pedipalp, regardless of whether they mate with newly moulted, defenceless females or with older mature females that often attack them. We determined experimentally that the death of males is triggered immediately upon insertion of the second palp, when males become unresponsive, and heartbeat ceases within minutes of insertion. We discuss the possible adaptive significance of programmed death during copulation, and argue that male death has evolved in a context other than sexual cannibalism.

Male copulation frequency, sperm competition and genital damage in the golden orb-web spider (Nephila plumipes)

“…Males of these species are typically cannibalised by the female during their second copulation, and male Argiope and L. hasselti are apparently physiologically incapable of using a palp more than once (Forster 1992;Sasaki and Iwahashi 1995;Andrade 1996;Foellmer and Fairbairn 2003;Herberstein et al 2005;Snow and Andrade 2005). Sexual cannibalism is also common in N. plumipes Elgar 2001, 2002;Elgar et al 2003b) but, unlike red-backs and Argiope, it is apparently not inevitable after the male's second copulation.…”

“…Monogyny may also be a typical consequence of sexual cannibalism (Fromhage et al 2005). For example, male orb-web spiders of the genus Argiope mate with a single female by making a single insertion with each of their pedipalps (intromittant organs), and will always fall victim to the sexually cannibalistic female after the second insertion (Sasaki and Iwahashi 1995;Foellmer and Fairbairn 2003). Similarly, male red-back spiders (Latrodectus hasselti) typically fall victim to the sexually cannibalistic female after the second insertion (Forster 1992).…”

Obligate male death and sexual cannibalism in dark fishing spiders

“…Nevertheless, the possibility remains that self-sacrifice in D. tenebrosus simply facilitates increased sperm transfer, with sexual cannibalism itself providing males no additional benefits. For example, sexual cannibalism might be an incidental consequence of spontaneous male death, which is triggered by the hydraulic expansion of the hematodochal bulb during copulation (Argiope aurantia; Foellmer & Fairbairn, 2003). More work is needed to fully explore these, and other, hypotheses.…”

“…Our research with D. tenebrosus thus far provides no evidence that obligate male death in D. tenebrosus is adaptive because the male's body functions as a whole-body mating plug (Foellmer & Fairbairn, 2003;Knoflach, 2004;Knoflach & van Harten, 2001). The body of a D. tenebrosus male curls up and hangs from the female's genital opening following copulation, introducing the potential to act as a whole-body mating plug (see Miller, 2007).…”

“…The second male was left in the arena with the female for up to 3 h. We chose a 30 min interval since females may encounter multiple males within a single night (Schwartz et al, 2013) and this time period enabled us to explore the potential for obligate male death to provide males an advantage in sperm competition through a whole-body mating plug (see Foellmer & Fairbairn, 2003;Knoflach & van Harten, 2001), a hypothesis independent of any adaptive significance of cannibalism (i.e. cannibalism is not necessary).…”